62 Scientific American, July 2013 Photograph by Tktk Tktk © 2013 Scientific American WhenANIMAL BEHAVIOR An mals Mournı Mounting evidence from species as diverse as cats and dolphins indicates that humans are not the only species that grieves over the loss of loved ones By Barbara J. King

n a research vessel in the waters off Greece’s Amvrakikos Gulf, Joan Gonzalvo watched a female bottlenose dolphin in obvious distress. Over and over Oagain, the dolphin pushed a newborn calf, almost certainly her own, away from the observers’ boat and against the current with her snout and pectoral fins. It was as if she wanted to nudge her baby into motion—but to no avail. The baby was dead. Float- ing under direct sunlight on a hot day, its body quickly began to decay; occasionally the mother removed pieces of dead skin and loose tissue from the corpse. When the female dolphin continued to behave in this way into a second day, Gonzalvo and his colleagues on the boat grew con- cerned: in addition to fussing with the calf, she was not eating nor- mally, behavior that could be risky for her health, given dolphins’ high metabolism. Three other dolphins from the Amvrakikos pop- ulation of about 150 approached the pair, but none disrupted the mother’s behavior or followed suit. As he watched the event unfold in 2007, Gonzalvo, a marine biologist at the Tethys Research Institute in Milan, Italy, decided he would not collect the infant’s body to perform a necropsy, as he would usually have done for research purposes. “What prompted me not to interfere was respect,” he told me earlier this year. “We

Illustration by Artist Name July 2013, ScientificAmerican.com 63 © 2013 Scientific American were privileged to be able to witness such clear evidence of the mother-calf bond in bottlenose dolphins, a species that I have Barbara J. King is a professor of anthropology at been studying for over a decade. I was more interested in observ- the College of William and Mary. Her studies of ing that natural behavior than interrupting it by abruptly inter- monkeys and apes have led her to examine emotion fering and disturbing a mother who was already in obvious dis- and intelligence in a wide range of animal species. tress. I would define what I saw as mourning.” Was the dolphin mother truly grieving for her dead calf? A decade ago I would have said no. As a biological anthropologist who studies animal cognition and emotion, I would have recog- nized the poignancy of the mother’s behavior but resisted inter- preting it as mourning. Like most animal behaviorists, I was To study and understand grief among animals, scientists need trained to describe such reactions in neutral terms such as a definition that distinguishes it from other emotions. Whereas “altered behavior in response to another’s death.” After all, the “animal response to death” embraces any behavior by an individ- mother might have become agitated only because the strange, ual following the death of a companion animal, researchers may inert status of her calf puzzled her. Tradition dictates that it is strongly suspect grief only when certain conditions are met. soft-hearted and unscientific to project human emotions such as First, two (or more) animals choose to spend time together grief onto other animals. beyond survival-oriented behaviors such as foraging or mating. Now, though, especially after two years’ research for my book Second, when one animal dies, the survivor alters his or her nor- How Animals Grieve, I think Gonzalvo was correct in his judg- mal behavioral routine—perhaps reducing the amount of time ment that the mother dolphin was mourning. In the past few devoted to eating or sleeping, adopting a body posture or facial years a critical mass of new observations of animal responses to expression indicative of depression or agitation, or generally fail- death has bubbled to the surface, leading me to a startling con- ing to thrive. For his part, Darwin conflated grief with sadness. clusion: cetaceans, great apes, elephants, and a host of other spe- But the two differ, primarily in intensity: the grieving animal is cies ranging from farm animals to domestic pets may, depending more acutely distressed, possibly for a more prolonged period. on circumstances and their own individual personalities, grieve This two-part definition is imperfect. For one thing, scientists when a relative or close friend dies. That such a broad range of lack a metric for evaluating exactly what counts as “more acutely species—including some quite distantly related to humans— distressed.” Should the criteria for grief differ according to spe- lament the passing of loved ones hints that the roots of our own cies, and might grief in other animals assume forms that are dif- capacity for grief run very deep indeed. ficult for humans to recognize as mourning? The data are not yet available on these questions. Furthermore, mothers or other DEFINING GRIEF caretakers that constantly provide food or protection to infants since charles Darwin’s Day, two centuries ago, scientists have that subsequently die cannot be said to have met the first criteri- debated hotly whether some animals display emotions beyond on (going beyond survival-oriented behaviors), yet they remain those associated with parental care or other aspects of survival among the strongest candidates for suffering survivor’s grief. and reproduction. Darwin thought that, given the evolutionary Future studies of animal mourning will help refine this defi- connection between humans and other animals, many emo- nition. For now, it furthers our critical assessment of responses tions must be similar across species. He granted to monkeys, for made by animals when others around them die. For instance, instance, grief and jealousy, as well as pleasure and vexation. baboon and chimpanzee mothers in wild African populations But the attribution of emotions such as these to animals fell sometimes carry the corpse of their dead babies for days, weeks increasingly out of mainstream scientific favor. By the early or even months—a behavior that on the surface of things might 20th century the behaviorist paradigm held sway, with its insis- look like grief. But they may not exhibit any significant outward tence that only observable behavior of animals, not their interi- indicator of agitation or distress. When the animals carry on or lives, could be studied with rigor. Gradually the scientific with their routine behaviors, such as mating, their behavior does embrace of animal emotion has revived, thanks originally in not meet the criteria for mourning. part to anecdotes from long-term field studies on large-brained mammals. From Tanzania, Jane Goodall recounted in heart- A MENAGERIE OF MOURNERS wrenching detail young chimpanzee Flint’s decline and death a wiDe range of species do exhibit behaviors that fit the two-part from grief only weeks after the death of his mother, Flo. From definition of grief, however, elephants among them. A particular- Kenya, Cynthia Moss reported that elephants attend to dying ly compelling example of elephant mourning comes from Iain comrades and stroke the bones of deceased relatives. Field biol- Douglas-Hamilton of Save the Elephants and his team at Kenya’s ogists and anthropologists began to ask questions about wheth- Samburu National Reserve, who in 2003 tracked elephants’ er, and how, animals mourn. responses to the dying matriarch called Eleanor. When Eleanor Getty Images Getty IN BRIEF

Animal behaviorists have traditionally shied away But a growing body of evidence indicates that spe- These observations suggest that although the ways from attributing human emotions, such as grief, to re- cies ranging from dolphins to ducks mourn the pass- in which we mourn may be uniquely human, our ca- sponses by animals. ing of relatives and close companions. pacity for grief has deep evolutionary roots. PRECEDING PAGES: TIM FLACH TIM FLACH PRECEDING PAGES:

64 Scientific American, July 2013 © 2013 Scientific American DOLPHIN MOTHER carries the body of her dead calf on her dorsal fin in the waters off Dana Point, Calif.

collapsed, a matriarch named Grace from another elephant fam- Giraffe Project, based in Kenya, never saw the mother more ily immediately came to her aid, using her tusks to support Elea- than 20 meters away. Although individuals in a giraffe herd nor back onto her feet. When Eleanor fell again, Grace stayed often synchronize their activities, foraging together, for exam- with her, pushing on her body, for at least an hour, even though ple, the mother deviated from this pattern, preferring to stay her own family moved on. Then Eleanor died. During the course close to the baby. Like the dolphin mother in the Amvrakikos of the week that followed, females from five elephant families, Gulf, she may have risked her own health in doing so—though including Eleanor’s own, showed keen interest in the body. Some in this case for a living offspring. individuals appeared upset, pulling at and nudging the body One day Muller discovered the herd engaged in highly atypi- with trunk and feet or rocking back and forth while standing cal behavior. Seventeen females, including the calf’s mother, over it. Based on the females’ reactions (at no point during this were vigilant and restless as they stared into a patch of bush. The period did a bull elephant visit the carcass), Douglas-Hamilton calf had died in that spot about an hour before. All 17 females concluded that elephants show a so-called generalized response showed keen interest in the body that morning, approaching to dying and death—grieving not only for the loss of close kin but and then retreating from it. By the afternoon 23 females and four

www.dolphinsafari.com for individuals in other families. juveniles were involved, and some nudged the carcass with their Wild cetaceans also seem to exhibit a generalized grief muzzles. That evening 15 adult females clustered closely around response. In the Canary Islands in 2001 Fabian Ritter of Mammal the body— more closely than they had been during the day. Encounters Education Research observed a rough-toothed dol- Throughout the following day numerous adult giraffes phin mother pushing and retrieving her dead calf’s body in attended the infant’s body. Some adult males approached for the much the same way that the Amvrakikos dolphin mother had first time, although they showed no interest in the carcass, with her baby’s corpse. She was not alone: two adult escorts instead focusing on foraging or inspecting the reproductive sta- swam synchronously with her at certain periods, and at other tus of the females. On day three Muller spotted the mother times a group of at least 15 dolphins altered their pace of travel to giraffe alone under a tree about 50 meters from where the calf include the mother and dead baby. The mother’s persistence was had died. The body itself, however, was no longer in its resting remarkable, and when on the fifth day it began to wane, the spot. Following a search, Muller located it, half-devoured, in the escorts joined in and supported the infant on their own backs. spot under the tree where the mother had been earlier. By the Giraffes, too, appear to grieve. In 2010 at the Soysambu Con- next day the body was gone, taken by hyenas. servancy in Kenya, a female Rothschild’s giraffe gave birth to a Giraffes are highly social animals. After caching a newborn baby with a deformed foot. The baby walked less and remained out of sight for about the first four weeks of life, the mothers more stationary than most calves. During the youngster’s four sometimes engage in a crèche system in which one looks after

COURTESY OF CAPTAIN DAVE’S DOLPHIN AND WHALE WATCHING SAFARI, DANA POINT, CALIF. CALIF. POINT, DANA SAFARI, WATCHING WHALE AND DOLPHIN DAVE’S CAPTAIN OF COURTESY weeks of life, wildlife biologist Zoe Muller of the Rothschild’s the infants while the others forage. Muller does not use the

July 2013, ScientificAmerican.com 65 © 2013 Scientific American words “grief” or “mourning” in describing the incident she witnessed. Yet this case is especially instructive. Not only the mother’s behavior but also that of many of the females in her herd changed significantly in the wake of the infant’s death. Although it is impossible to rule out an alternative explanation, the fact that the females had mounted a protective response against pred- ators taking the baby makes it overwhelmingly likely that grief was involved at some level. Detailed observations of wild populations of ani- mals, such as the ones Muller reported, are still rela- tively rare, for several reasons. Scientists may not be at the right place at the right time to observe post- death responses by survivors. And even when they are present, no remarkable grief behaviors may ensue. Especially at this early stage of research into animal grief, observations from sanctuaries, zoos and even our own homes may supply needed clues. I cannot imagine describing the behavior of Willa the Siamese cat without invoking the word “grief.” For 14 years Willa lived with her sister, Carson, at the home of Karen and Ron Flowe in Virginia. The feline siblings groomed each other, lazed together in favorite parts of the house and slept with their bodies entwined. If Carson was taken from the house to visit the vet, Willa acted mildly agitated until she reunited with her sister. In 2011 Carson’s chronic medical issues wors- ened, and the Flowes took her again to the vet, where she died in her sleep. At first, Willa acted as she did when her sister was away for a brief period. Within two or three days, though, she began to utter an unearthly sound, a sort of wail, FEMALE GORILLA clutches her dead baby in a zoo in Münster, and to search the spots she and Carson had Germany. Although such behavior is not sufficient to demonstrate favored together. Even when this startling behav- mourning, mothers who lose infants are among the strongest candidates ior faded, Willa remained lethargic for months. for experiencing survivor’s grief. Of all the instances of animal grief I have com- piled, the most surprising came from a sanctuary setting. In 2006 three mulard ducks arrived at Farm Sanctuary communities may more readily mourn the deaths of loved ones in Watkins Glen, N.Y. They suffered from hepatic lipidosis, a liver than other species do. But researchers do not yet know enough disease caused by force-feeding of the birds at a foie gras farm. about animal grief to make such a claim. We need to test this Two of the rescued ducks, Kohl and Harper, were in bad shape hypothesis by systematically comparing responses to death in a physically and emotionally. Very afraid of people, Kohl had variety of animal social systems, from gregarious ones to those in deformed legs and Harper was blind in one eye. The two forged a which animals come together only seasonally for food or mating. fine supportive friendship for four years. Ducks are social birds, Still, species-level differences in grieving will not be the but even so, the intensity of their bond was unusual. When Kohl’s whole story, because variation in the immediate social contexts leg pain increased and he could no longer walk, he was eutha- and personalities of individual survivors will complicate mat- nized. Harper was allowed to observe the procedure and to ters. For instance, whereas the practice of allowing a survivor to approach his friend’s body afterward. After pushing on the body, view the body, as Harper did with Kohl, sometimes seems to pre- Harper laid down and put his head and neck over Kohl’s neck. vent or reduce a period of distressed searching and vocalizing by There he stayed for some hours. In effect, Harper never recov- the surviving animal, other times it seems not to help at all— ered from his loss. Day after day, he snubbed other potential attesting to the degree of individual variation in death responses duck friends, preferring to sit near a small pond where he had within species. Likewise, evidence for grief in wild monkeys that often gone with Kohl. Two months later Harper died as well. live in cohesive social units is surprisingly limited so far, whereas

in more solitary species such as domestic cats, bonds may devel- Images Getty THE SORROW CONTINUUM op be tween two or more kin or friends such that grief responses it is logical to think that long-lived species whose members part- rival those of much more social animals. I would predict that

ner most closely with others in tight-knit pairs, family groups or field observations will show that some monkeys across varied OLIVER WERNER

66 Scientific American, July 2013 © 2013 Scientific American social systems visibly mourn as much as some domestic cats. Mom and rolled over exuberantly at her feet. Then Mom left for Indeed, in How Animals Grieve, I recount examples from cats, good. Some of the coyotes in her pack paced; others searched for dogs, rabbits, horses and birds, as well as the other animals dis- her, setting off in the direction Mom had departed. “For more cussed here. In each species I find a grief continuum, with some than a week some spark seemed to be gone,” Bekoff writes. “Her individuals seeming indifferent to a companion’s death and oth- family missed her.” Discussing animal emotion with me earlier er individuals appearing distraught over such a loss. this year, Bekoff attributed the family’s response to its love for Cognitive differences also play a role in animal grief. Just as Mom. Generally, the potential for love is strong in species such as there are different levels of empathy expressed by different spe- coyotes, wolves and many birds, including geese, he said, because cies and even across individuals within a species, there must be male and female partners defend territories, feed and raise their varying levels of comprehension when animals grieve. Do some young together, and miss each other when they are apart. Love in the animal world often entwines with grief in an acute mutuality. Perhaps even more than the degree of social cohesion within a spe- Love in the animal world cies, it is love between individuals that predicts when grief will be expressed. Can there be any often entwines with grief real doubt that Willa, a representative of a spe- cies (the domestic cat) not known for its social in an acute mutuality. nature, loved her sister, Carson, or that as the sole surviving sister, she suffered grief in the wake of her loss? animals grasp death’s finality or even have a mental concept of In our own species, grief increasingly became expressed death? We simply don’t know. No evidence suggests that any through rituals rich in symbolism. By around 100,000 years ago, nonhuman animal anticipates death in the way we humans do, a our Homo sapiens ancestors decorated dead bodies in red ocher, capacity that underlies so much of our compelling literature, a behavior interpreted by archaeologists to be a kind of symbolic music, art and theater—and that costs our species a great deal in (rather than functional) ornamentation. At a site in Russia called terms of emotional suffering. Sunghir, two children younger than 13 years, a boy and a girl, Indeed, the capacity to mourn may become quite costly for were buried 24,000 years ago, together with elaborate grave any animal in both physical and emotional terms, especially in goods ranging from mammoth tusks to animals carved from ivo- the wild where alert high-energy behavior is needed for foraging, ry. Most astonishing were the thousands of ivory beads found in predator avoidance and mating. Why then did grief evolve in the the pair’s grave, probably sewn onto the clothing (long since dis- first place? Perhaps the social withdrawal that often accompa- integrated) in which the children were buried. A good portion of nies an animal’s grief, if not taken too far, allows time for rest this ancient human community at Sunghir must have come and thus an emotional recovery that in turn leads to greater suc- together in preparing this funeral ritual—each bead alone took cess in forging a new close bond. Or, as John Archer writes in The an hour or more to manufacture. Although it is risky to project Nature of Grief, it may be that “the costs involved in grief can be modern emotions onto past populations, the examples of animal viewed as a trade-off with the overall benefits conferred by sepa- grief reviewed here strengthen an emotion-based interpretation ration responses” seen when two individuals are keenly attached of the archaeological evidence: our ancestors of many thousands but forced apart from each other. Under such circumstances, the of years ago mourned their lost children. missing partners may search for each other and thereby reunite In our modern world, grief is no longer inevitably confined to and live to see another day. What is adaptive, then, may not be kin, close social partners or immediate members of one’s own grief itself but instead the strong positive emotions experienced community. Public commemoratives at the Peace Memorial Park before grief comes into the picture, shared between two or more in Hiroshima; the genocide memorial center in Kigali, Rwanda; living animals whose level of cooperation in nurturing or the Foundation Memorial to the Murdered Jews of Europe in resource-acquisition tasks is enhanced by these feelings. Berlin; or the site of the Twin Towers in Manhattan or Sandy Hook Elementary School in Newtown, Conn., all convey visibly THE PRICE OF LOVE the power of agonized global mourning. Our uniquely human From this perspective, we may link grief with love, full stop. That capacity for sorrow at the deaths of those who are strangers to us is to say, grief results from love lost. Exploring emotions in a vari- is built on an evolutionary substrate. Our own ways of mourning ety of species, ecologist and animal behaviorist Marc Bekoff of the may be unique, but the human capacity to grieve deeply is some- University of Colorado at Boulder embraces the idea that many thing we share with other animals. animals feel “love” as well as “grief,” even as he acknowledges that those concepts are hard to define precisely. We humans, he MORE TO EXPLORE notes, do not fully understand love, but we do not deny its exis- tence—or its power to shape our emotional responses. Animals Matter: A Biologist Explains Why We Should Treat Animals with Compassion and Respect. Mark Bekoff. Shambhala, 2007. In his book Animals Matter, Bekoff tells the story of a coyote How Animals Grieve. Barbara J. King. University of Chicago Press, 2013. called Mom whom he observed for several years during behavior- SCIENTIFIC AMERICAN ONLINE al studies in Wyoming’s Grand Teton National Park. At one point For examples of animal responses to death that do not qualify as grief, Mom began to make short journeys on her own away from her go to ScientificAmerican.com/jul2013/grief pack. Her offspring would rejoice when she returned: they licked

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